usually precipitate the quarantine and shipping restrictions associated with such insect pests as Mediterranean fruit fly. Furthermore, tools typically employed for early detection of low insect population densities, such as pheromone or bait traps, are not available for whiteflies, and newly introduced whiteflies are often wide- spread before they are discovered. Conse- quently, modern strategies for managing populations of exotic whitefly pests typi- cally center around biological control rather than eradication. The history of Siphoninus phillyreae (Haliday)in North America typifies many introduced whiteflies. Siphoninus phillyreae is an Old World species, reported in the Eastern Hemisphere from Morocco to In- dia, and from Ireland to Central Africa. Its discovery in California was the first re- corded in the Western Hemisphere. In the absence of effective natural enemies in California, this whitefly subsequently de- veloped extensive, damaging populations. Siphoninus phillyreae whitefly develops continuously, although more slowly dur- ing cooler (winter) temperatures, complet- ing several generations each year. In heavily infested areas populations rapidly occupy undersides of all leaves on suscep- tible trees. Nymphal populations on trees cause premature dehiscence of leaves and defoliation, severely reduce yield in fruit trees and, in some cases, cause the death of young pear trees following repeated defo- liation. Honeydew produced by whiteflies falls on sidewalks, lawns and automobiles, and is carried by air currents and foot traf- fic into homes, causing sticky furniture, draperies and carpets. It further serves as a medium for sooty molds, which discolor any surface affected by the honeydew, in- cluding fruit intended for market. Adult populations reach astounding levels, limit- ing outdoor activity in many areas. Princi- Biological control pally affected are ornamental shade trees as well as pomegranate, apple, pear, citrus and, to a lesser degree, stone fruits. Infes- of ash whitefly: tations affect not only agricultural produc- tion but also dramatically affect the quality a success in progress of life in urban communities. The biological control program em- ployed exemplifies the approaches suit- Tom S. Bellows P Timothy D. Paine o Juli R. Gould able for limiting the impact of many pests Larry G. Bezark P Joe C. Ball* introduced in urban and agricultural set- tings. These approaches include (1)detec- Two natural enemies of ash white- Exotic whiteflies have long threatened tion of the pest and mounting of a biologi- fly (Siphoninus phillyreae), jntro- California’s farms and gardens. At least cal control program, (2)foreign explora- eight species are established in the state; tion and introduction of exotic natural duced into California in 1990, several more recognized pest species exist continued on p. 27 proved effective in Southern Cali- in other Western Hemisphere areas and in fornia field trials, completely con- regions bordering the Pa’cific Basin. trollina this Dest in ‘release sites Damage to plants is typically related to within-z4 mbnths, Evaluations in large populations feeding-on leaves and to production of large quantities of honey- release sites in Central and North- dew, Because typically do not ern California, Arizona and Nevada infest fruits, the presence of a particular look equally promising. species in & agkultural regiin does not

24 CALIFORNIA AGRICULTURE, VOLUME 46, NUMBER 1 continued from p. 24 enemies, (3) evaluation of natural enemy potential and (4)regionwide distribution of natural enemies. The problem Siphoninus phillyreae was first identified in California in Los Angeles in August 1988. The infestation was widespread in Los Angeles, Orange and San Bemardino counties, and high densities in some areas indicated that the infestation had existed for one or two seasons before 1988. The in- festation spread rapidly, and now this whitefly is found in nearly every county in California; infestations are also reported in Nevada, Arizona and New Mexico. Fol- lowing meetings with agricultural com- missioners and state agricultural officials in January and February 1990, initial fund- ing for establishing a biological control creased production of adult whiteflies, Larval (above)and adult (below)forms of the ladybird beetle Clitosfefhus arcuafus, an ash program at the University of California densities of 5. phillyreae, which had been whitefly predator. was secured from UC funds, agricultural increasing in the absence of E. partenopea, commodity boards, county boards of su- began to decline. By October 1990, the pervisors, and the California Department density of 5. phillyreae had been reduced of Food and Agriculture (CDFA). 13-fold.Densities of S. phillyreae continued to drop in 1991, and by September 1991, Natural enemies found, introduced whitefly densities were between 3 and 4 During 1989 and 1990, T. Bellows, (UC orders of magnitude or 1,000 to 10,000 Riverside), L. Bezark (CDFA) and D. times lower than they had been at the Gerling (University of Tel Aviv) intro- peak in 1990 (fig. 1).Emergence of E. duced nine populations of natural enemies partenopea continued to constitute 80 to into UC Riverside quarantine facilities. 98% of the total emergence of whiteflies Three populations reproduced in quaran- and parasites from 5. phillyreae nymphs. tine: the tiny parasitic wasp Encarsia Densities of 5. phillyreae were so low in purtenopeu from Italy, E. partenopea from Is- 1991 that the whitefly is now difficult to rael, and the predaceous ladybird beetle find in Riverside and in most other parts Clitostethus arcuatus from Israel. Initial of Southern California. The wasp was dis- shipments were received in late summer tributed in summer 1990 in several loca- matic regions throughout infested por- 1989 and, following clearance through tions in Los Angeles, San Bernardino, Riv- tions of the state. Releases were made in quarantine protocols, the first releases of erside, Orange and San Diego counties, Alameda, Fresno, Kern, Los Angeles, Sac- wasps from Israel were made in October and results in these locations were similar ramento, Santa Barbara, Stanislaus, Tulare, 1989; first recoveries were made approxi- to those obtained in Riverside. Ventura and Yolo counties during Sep- mately 6 weeks later. The beetle was re- tember and October 1990; subsequent re- leased first in spring 1990 in coastal San Regionwide evaluation leases were made beginning in June 1991. Diego County where it, too, became estab- The wasp E. partenopea and the beetle The parasite became established in all lished. Early results from the wasp re- C. arcuatus from Israel were distributed in counties (fig. 21, but establishment of the leases were encouraging, and during the several whitefly-infested areas in 1990 to beetle was less uniform. Populations be- winter, colonies of the wasp from Israel evaluate the overwintering ability and came established following releases in were.developed and expanded. subsequent level of biological control Hayward (on San Francisco Bay), achieved by these natural enemies in cli- Modesto, Fresno, Davis and Ventura, but Initial research: parasitic wasp not in Pleasanton, Bakersfield or Ojai. Experiments were conducted in River- More research will reveal whether the side in summer 1990 to assess the effect of beetle will eventually establish in these lo- E. partenopea on populations of S. cations. phillyreae. At sites where parasites were re- During 1991, a few city governments leased in May, densities of the whitefl7 re- contracted UC to distribute and evaluate mained below 8 immature insects/cm the natural enemies in their areas, and this (52/in2).In contrast, whiteflies were in- work was conducted in cooperation with creasing in density during early summer local Cooperative Extension personnel. In at nonrelease sites. Nonrelease sites did 30May 7Sept 23Aug 1 Dec addition, during 5 weeks in summer 1991, 1990 1991 not remain free of parasites for long, how- Date more than 100,000 wasps were distributed ever, even though they were up to 11 km to public agencies and private individuals, Fig. 1. Changes in density of immature ash (7 miles) from release sites. Once the para- whitefly (Siphoninus phillyreae) and percent- primarily in Southern California and, in site entered a population, the percentage age of whitefly pupae producing parasitic smaller numbers, to locations as far north of whitefly nymphs producing E. wasps (Encarsiaparfenopea) rather than adult as Yolo County. partenopea, rather than adult whiteflies, whiteflies on pomegranate in Riverside, 1990- Releases of E. purtenopeu had substantial rapidly increased (fig. 1). As a result of de- 1991. impacts on the populations of 5. phillyreae

CALIFORNIA AGRICULTURE, JANUARY-FEBRUARY 1992 27 70% covered by all whitefly stages. How- by UC and state and federal resources to ever, on August 2, an average of 408 para- maintain the personnel and facilities nec- sites were counted in a similar sampling essary to conduct such programs. Facilities period on leaves in Modesto. Only 40% of such as the quarantine laboratory and the the leaves contained whitefly life stages. Department of Entomology at UC River- The adult population of parasites was 10- side are critical to maintaining biological fold larger and the level of damage was al- control programs. most 60% lower in Modesto, which ini- Furthermore, there were substantial tially released a larger number of natural commitment and assistance from col- enemies, began releases at an earlier date leagues in California and overseas to de- and subsequently redistributed the para- velop the program. This assistance was the sites. result, over many years, of networking by The wasp has now been distributed, researchers addressing similar problems through both UC programs and state pro- in similar ways, and represents a vital, and grams, in varying numbers throughout in- often unappreciated, dividend from the fested regions of California, and through maintenance of academic and research in- UC programs also to Arizona and Nevada. stitutions. These factors allow UC to re- It appears to function well in all the cli- spond rapidly, and often successfully,to mate zones into which it has been intro- new invasions. duced, including the deserts of California Exotic whiteflies have persisted in Cali- and Arizona, Californian coastal climates, fornia, but biological control has helped Fig. 2. Release locations of the parasitic wasp and interior valleys, from Mexico to north- manage four of the eight species present. €marsh partenopea and the predaceous em Central California. This parasite will Other whitefly species that threaten both beetle Clitostethus arcuatus. Each point indi- likely play a major role in limiting S. urban and agncultural communities, but cates one or more release locations at each phillyreae populations in all of these areas. are not now in California, are the orange study site. The hollow triangles in Kern, spiny whitefly, currently in Southeast Ventura and Alameda counties indicate loca- Outlook Asia; the spiralling whitefly, currently in tions where no establishment was apparent af- ter single releases of the beetle. The biological control program against Florida, the Caribbean and Hawaii; and S. phillyreae exemplifies several character- the citrus blackfly, currently in Florida, by the end of summer 1991 in all locations. istics vital to modem, effective use of bio- Texas, the Caribbean and Mexico. Other For example, by October virtually all of logical control as a management tool exotic whiteflies present in California are the whitefly fourth instar nymphal exu- against invading, exotic pest species. It is being evaluated for their impact and can- viae examined in Santa Barbara had evi- perhaps one of the most visible examples didacy for biological control. (The outlook dence of emergence of parasites rather of biological control in an urban setting for one of these, the sweetpotato whitefly, than adult whiteflies. There was little defo- and exemplifiesthe potential sigruficance is described in the accompanying sidebar.) liation of trees in Modesto at the initial of this approach to managing pests in ur- ~ ~~~ ~~ ~~ parasite release sites and surrounding ban landscapes. T. S. Bellows is Associate Professor, T. D. neighborhoods, although defoliation did Signhcant in the program’s develop- Paine is Assistant Professor, and J. R. Gould is occur at sites where the parasite appeared ment was early participation by several Postgraduate Research Associate, all at UC much later in the season. Parasitism rates funding agencies, which included not only Riverside; L. G. Bezark and J. Ball are Envi- were substantial in every release site ex- commodity groups concerned about the ronmental Research Scientists, Department of amined throughout California. impact to agriculture, but also several civic Pesticide Regulation, Cal-EPA; W. Bentley is The number of parasites released in a governmental organizations, particularly Farm Advisor, Kern County; R. Coviello is particular location affected the rate of county agricultural commissioner’s offices Farm Advisor, Fresno County; J. Downer is population growth and spread. The cities and county boards of supervisors. Support Farm Advisor, Ventura County; P. Elam is of Modesto and Fresno present two differ- from local governmental organizations Farm Advisor, Fresno County; D. Flaherty is ent philosophies and patterns of establish- may play a critical role in developing fu- retired Farm Advisor, Tulare County; P. ment. Both cities received the same initial ture biological programs affecting urban Gouveia is IPM Specialist, Parks Department, number of parasites (750) as part of the UC environments.Many pests of urban and City of Davis; C. Koehler is retired Specialist, project (plus an additional 250 individuals periurban settings, such as those of orna- UC Berkeley; R. Molinar is Farm Advisor, as part of the CDFA distribution to coun- mental landscapes, may not precipitate Alameda County; N.O’Connell is Farm Advi- ties statewide).In addition, the Parks and concerns or support for research from ag- sor, Tulare County; E. Perry is Farm Advisor, Recreation Department of Modesto ac- ricultural industries, but are eminently Stanislaus County, and Greg Vogel is Farm quired 5,000 parasites in May and another suitable candidates for biological control. Advisor, Sacramento County. 5,000 in July 1991 from UC. These wasps The success of, and rate of implementation The authors thank Prof. D. Gerling and were initially released at parasite nursery of, biological control in urban environ- Prof. G. Viggiani and Drs. K. Hopper, A. Kirk sites. Their progeny were collected and ments will depend partly on continued in- and L. Knutson for their assistance in obtain- uniformly redistributed on a quarter-mile volvement by local and state governments ing natural enemies of Siphoninus philly- grid throughout the city. In Fresno, indi- in representing the pest control interests of reae. This project was supported in part by vidual citizens acquired 3,000 E. partenopea urban residents. grants from California Tree Fruit Agreement, in July for release on private landscapes. Additionally, among the important California Pistachio Commission, California Adult parasites were first detected in characteristics of this program were the fa- Association of Nurserymen, California Nurs- samples taken in Modesto on June 18, but cilities of UC Riverside with its capabilities ey Growers Association, Citrus Research not until August 22 in Fresno. For further in biological control. Biological control has Board, University of California IPM Program, comparison, 46 parasites were counted in occupied a central place in California pest the International Society of Arboriculture, and a 5-minute visual-sampling period on the management strategies for decades, and the Agricultural Commissioner’s ofices of San underside of host tree leaves on August 27 this heritage has been the result of careful Diego, Orange, Los Angeles, Riverside and in Fresno, and lower leaf surfaces were program development and a commitment Santa Barbara counties.

28 CALIFORNIA AGRICULTURE, VOLUME 46, NUMBER 1